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Coordinate regulation of ribosomal protein (RP) genes is key for controlling cell growth. Although several transcriptional regulators of RPs have been identified, we have a limited understanding of how regulation is encoded within RP promoters. For example, many RP genes in yeast exist in duplicate copies but some have only one copy, and it is not clear how proper RP stoichiometry is achieved in light of these copy-number differences. We fused 110 different RP promoters from yeast to a fluorescent gene reporter, allowing us to robustly detect differences in their promoter transcription rates that are as small as ~10%. We found that single-copy RP promoters have significantly higher transcription rates, suggesting that proper RP stoichiometry is partly encoded within RP promoter sequences. Notably, RP promoters with higher transcription rates have more nucleosome-disfavoring sequences, and characteristic spatial organizations of these sequences and of binding sites for key regulators. A computational model that incorporates both transcription factors and nucleosomes explains a large fraction of the variability in RP transcription rates. Thus, our results partly uncover how RP regulation is achieved and suggest that DNA-encoded nucleosome organization of promoters may be a key mechanism by which genomes encode biologically meaningful transcription rates. Our approach can readily be applied to uncover how transcriptional programs of other promoters are encoded.